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Birds have paedomorphic dinosaur skulls


The interplay of evolution and development has been at the heart of evolutionary theory for more than a century1. Heterochrony—change in the timing or rate of developmental events—has been implicated in the evolution of major vertebrate lineages such as mammals2, including humans1. Birds are the most speciose land vertebrates, with more than 10,000 living species3 representing a bewildering array of ecologies. Their anatomy is radically different from that of other vertebrates. The unique bird skull houses two highly specialized systems: the sophisticated visual and neuromuscular coordination system4,5 allows flight coordination and exploitation of diverse visual landscapes, and the astonishing variations of the beak enable a wide range of avian lifestyles. Here we use a geometric morphometric approach integrating developmental, neontological and palaeontological data to show that the heterochronic process of paedomorphosis, by which descendants resemble the juveniles of their ancestors, is responsible for several major evolutionary transitions in the origin of birds. We analysed the variability of a series of landmarks on all known theropod dinosaur skull ontogenies as well as outgroups and birds. The first dimension of variability captured ontogeny, indicating a conserved ontogenetic trajectory. The second dimension accounted for phylogenetic change towards more bird-like dinosaurs. Basally branching eumaniraptorans and avialans clustered with embryos of other archosaurs, indicating paedomorphosis. Our results reveal at least four paedomorphic episodes in the history of birds combined with localized peramorphosis (development beyond the adult state of ancestors) in the beak. Paedomorphic enlargement of the eyes and associated brain regions parallels the enlargement of the nasal cavity and olfactory brain in mammals6. This study can be a model for investigations of heterochrony in evolutionary transitions, illuminating the origin of adaptive features and inspiring studies of developmental mechanisms.

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Figure 1: Archosaur phylogeny and ontogeny.
Figure 2: PCA plot with outline images of hypothetical extremes along each axis, set on deformation grids from average.
Figure 3: Summary of ontogenetic changes in archosaur skulls; outlines on deformation grids from average.
Figure 4: Similarity of embryonic Alligator and adult Confuciusornis skulls.
Figure 5: Summary of heterochrony and phylogeny in bird skull evolution.
Figure 6


  1. Gould, S. J. Ontogeny and Phylogeny (Belknap, 1977)

    Google Scholar 

  2. Rowe, T. Coevolution of the mammalian middle ear and neocortex. Science 273, 651–654 (1996)

    Article  ADS  CAS  Google Scholar 

  3. Gill, F. B. Ornithology (Freeman, 2006)

    Google Scholar 

  4. Nieuwenhuys, R., Ten Donkelaar, H. J. & Nicholson, C. The Central Nervous System of Vertebrates (Springer, 1998)

    Book  Google Scholar 

  5. Butler, A. B. & Hodos, W. Comparative Vertebrate Neuroanatomy (Wiley, 1996)

    Google Scholar 

  6. Rowe, T. B., Macrini, T. E. & Luo, Z.-X. Fossil evidence on origin of the mammalian brain. Science 332, 955–957 (2011)

    Article  ADS  CAS  Google Scholar 

  7. Nesbitt, S. J. The early evolution of archosaurs: relationships and the origin of major clades. Bull. Am. Mus. Nat. Hist. 352, 1–292 (2011)

    Article  Google Scholar 

  8. Erickson, G. M. et al. Was dinosaurian physiology inherited by birds? Reconciling slow growth in Archaeopteryx . PLoS ONE 4, e7390 (2009)

    Article  ADS  Google Scholar 

  9. Wellnhofer, P. Archaeopteryx: The Icon of Evolution (Verlag Dr Friedrich Pfeil, 2009)

    Google Scholar 

  10. Jollie, M. T. The head skeleton of the chicken and remarks on the anatomy of this region in other birds. J. Morphol. 100, 389–436 (1957)

    Article  Google Scholar 

  11. Jerison, H. J. Evolution of the Brain and Intelligence (Academic, 1973)

    Google Scholar 

  12. Pearson, R. The Avian Brain (Academic, 1972)

    Google Scholar 

  13. Thulborn, R. A. Theropod dinosaurs, progenesis and birds: homology of digits in the manus. Neues Jb. Geol. Paläontol. Abh. 242, 205–241 (2006)

    Article  Google Scholar 

  14. Alonso, P. D., Milner, A. C., Ketcham, R. A., Cookson, M. J. & Rowe, T. B. The avian nature of the brain and inner ear of Archaeopteryx . Nature 430, 666–669 (2004)

    Article  ADS  CAS  Google Scholar 

  15. Brusatte, S. L., Sakamoto, M., Montanari, S. & Harcourt Smith, W. E. H. The evolution of cranial form and function in theropod dinosaurs: insights from geometric morphometrics. J. Evol. Biol. 25, 365–377 (2011)

    Article  Google Scholar 

  16. Padian, K., De Ricqlès, A. & Horner, J. R. Dinosaurian growth rates and bird origins. Nature 412, 405–408 (2001)

    Article  ADS  CAS  Google Scholar 

  17. Alberch, P., Gould, S. J., Oster, G. F. & Wake, D. B. Size and shape in ontogeny and phylogeny. Paleobiology 5, 296–317 (1979)

    Article  Google Scholar 

  18. Turner, A. H., Pol, D., Clarke, J. A., Erickson, G. M. & Norell, M. A. A basal dromaeosaurid and size evolution preceding avian flight. Science 317, 1378–1381 (2007)

    Article  ADS  CAS  Google Scholar 

  19. Lu, J., Unwin, D. M., Jin, X., Liu, Y. & Ji, Q. Evidence for modular evolution in a long-tailed pterosaur with a pterodactyloid skull. Proc. R. Soc. B 277, 383–389 (2010)

    Article  Google Scholar 

  20. Rowe, T. Definition, diagnosis, and origin of Mammalia. J. Vertebr. Paleontol. 8, 241–264 (1988)

    Article  Google Scholar 

  21. Kielan-Jaworowska, Z., Cifelli, R. L. & Luo, Z.-X. Mammals From the Age of Dinosaurs: Origins, Evolution, and Structure (Columbia Univ. Press, 2004)

    Book  Google Scholar 

  22. Fink, W. L. The conceptual relationship between ontogeny and phylogeny. Paleobiology 8, 254–264 (1982)

    Article  Google Scholar 

  23. Northcutt, R. G. Evolving large and complex brains. Science 332, 926–927 (2011)

    Article  ADS  CAS  Google Scholar 

  24. Hopson, J. A. Relative brain size and behavior in nonavian reptiles. Annu. Rev. Ecol. Syst. 8, 429–448 (1977)

    Article  Google Scholar 

  25. Hu, D. & Marcucio, R. S. A SHH-responsive signaling center in the forebrain regulates craniofacial morphogenesis via the facial ectoderm. Development 136, 107–116 (2009)

    Article  CAS  Google Scholar 

  26. Norell, M. A. et al. A review of the Mongolian Cretaceous dinosaur Saurornithoides (Troodontidae: Theropoda). Am. Mus. Novit. 3654, 1–63 (2009)

    Article  Google Scholar 

  27. Clarke, J. A. & Middleton, K. M. Mosaicism, molecules, and the evolution of birds: results from a Bayesian approach to the study of morphological evolution using discrete character data. Syst. Biol. 57, 185–201 (2008)

    Article  Google Scholar 

  28. Hunt, G. R. Manufacture and use of hook-tools by New Caledonian crows. Nature 379, 249–251 (1996)

    Article  ADS  CAS  Google Scholar 

  29. Smith, K. K. Time’s arrow: heterochrony and the evolution of development. Int. J. Dev. Biol. 47, 613–621 (2003)

    PubMed  Google Scholar 

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We thank R. M. Elsey and colleagues at the Rockefeller Wildlife Refuge, Louisiana Department of Wildlife and Fisheries for assistance in obtaining alligator embryos, S. Majadla for imaging assistance, C. Sánchez for constructing the Supplementary Movie, I. Sarris for assistance with the R script packages, and J. B. Losos, H. E. Hoekstra, F. A. Jenkins Jr and B. Zweig for comments that improved the manuscript. B.-A.S.B. was partly funded by National Science Foundation dissertation improvement grant 1110564. J.M.-L. was supported by project BFU2008-00642.

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Authors and Affiliations



B.-A.S.B. and A.A. designed the study. B.-A.S.B. wrote the paper and performed CT scans, data entry and analytical work. J.M.-L. performed analytical work and assisted with writing and figures. F.R. performed data entry and analytical work. G.B. helped conceive the project and performed data processing on new CT data. T.B.R. contributed CT data and assisted in data interpretation and writing the paper. M.A.N. contributed the major hypotheses to be tested, provided CT data and assisted in writing the paper. A.A. co-wrote the paper.

Corresponding authors

Correspondence to Bhart-Anjan S. Bhullar or Arhat Abzhanov.

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Supplementary Information

This file contains Supplementary Data 1-13, which comprises: Supplementary Text (1-9) and (11); Supplementary Figures 1-10 (10); Supplementary Methods and Supplementary Tables 1-4 (12); and Supplementary References (13) = – see Contents for details. Page 2 contains instructions for the Supplementary Animation files (see separate zipped files). (PDF 3234 kb)

Supplementary Animation

This zipped file contains a flash animation file (.swf) and a zipped file, which contains the ‘ontology.htm’ and ‘ontology.swf’ files. Instructions on how to open these files is given on page 2 of the Supplementary Information file. (ZIP 2360 kb)

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Bhullar, BA., Marugán-Lobón, J., Racimo, F. et al. Birds have paedomorphic dinosaur skulls. Nature 487, 223–226 (2012).

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